Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution

The lobe-finned fish, lungfish (Dipnoi, Sarcoptergii), have persisted for ~400 million years from the Devonian Period to present day. The evolution of their dermal skull and dentition is relatively well understood, but this is not the case for the central nervous system. While the brain has poor pre...

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Main Authors: Alice M Clement, Tom J Challands, Richard Cloutier, Laurent Houle, Per E Ahlberg, Shaun P Collin, John A Long
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/73461
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author Alice M Clement
Tom J Challands
Richard Cloutier
Laurent Houle
Per E Ahlberg
Shaun P Collin
John A Long
author_facet Alice M Clement
Tom J Challands
Richard Cloutier
Laurent Houle
Per E Ahlberg
Shaun P Collin
John A Long
author_sort Alice M Clement
collection DOAJ
description The lobe-finned fish, lungfish (Dipnoi, Sarcoptergii), have persisted for ~400 million years from the Devonian Period to present day. The evolution of their dermal skull and dentition is relatively well understood, but this is not the case for the central nervous system. While the brain has poor preservation potential and is not currently known in any fossil lungfish, substantial indirect information about it and associated structures (e.g. labyrinths) can be obtained from the cranial endocast. However, before the recent development of X-ray tomography as a palaeontological tool, these endocasts could not be studied non-destructively, and few detailed studies were undertaken. Here, we describe and illustrate the endocasts of six Palaeozoic lungfish from tomographic scans. We combine these with six previously described digital lungfish endocasts (4 fossil and 2 recent taxa) into a 12-taxon dataset for multivariate morphometric analysis using 17 variables. We find that the olfactory region is more highly plastic than the hindbrain, and undergoes significant elongation in several taxa. Further, while the semicircular canals covary as an integrated module, the utriculus and sacculus vary independently of each other. Functional interpretation suggests that olfaction has remained a dominant sense throughout lungfish evolution, and changes in the labyrinth may potentially reflect a change from nektonic to near-shore environmental niches. Phylogenetic implications show that endocranial form fails to support monophyly of the ‘chirodipterids’. Those with elongated crania similarly fail to form a distinct clade, suggesting these two paraphyletic groups have converged towards either head elongation or truncation driven by non-phylogenetic constraints.
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spelling doaj.art-fe0fbc43c02249cabc36f012098fb7b42022-12-22T03:50:52ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.73461Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolutionAlice M Clement0https://orcid.org/0000-0003-0380-7347Tom J Challands1Richard Cloutier2Laurent Houle3Per E Ahlberg4https://orcid.org/0000-0001-9054-2900Shaun P Collin5John A Long6https://orcid.org/0000-0001-8012-0114College of Science and Engineering, Flinders University, Adelaide, AustraliaSchool of Geosciences, University of Edinburgh, Edinburgh, United KingdomDépartement de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, CanadaDépartement de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, CanadaSubdepartment of Evolution and Development, Department of Organismal Biology, Uppsala University, Uppsala, SwedenSchool of Life Sciences, La Trobe University, Melbourne, AustraliaCollege of Science and Engineering, Flinders University, Adelaide, AustraliaThe lobe-finned fish, lungfish (Dipnoi, Sarcoptergii), have persisted for ~400 million years from the Devonian Period to present day. The evolution of their dermal skull and dentition is relatively well understood, but this is not the case for the central nervous system. While the brain has poor preservation potential and is not currently known in any fossil lungfish, substantial indirect information about it and associated structures (e.g. labyrinths) can be obtained from the cranial endocast. However, before the recent development of X-ray tomography as a palaeontological tool, these endocasts could not be studied non-destructively, and few detailed studies were undertaken. Here, we describe and illustrate the endocasts of six Palaeozoic lungfish from tomographic scans. We combine these with six previously described digital lungfish endocasts (4 fossil and 2 recent taxa) into a 12-taxon dataset for multivariate morphometric analysis using 17 variables. We find that the olfactory region is more highly plastic than the hindbrain, and undergoes significant elongation in several taxa. Further, while the semicircular canals covary as an integrated module, the utriculus and sacculus vary independently of each other. Functional interpretation suggests that olfaction has remained a dominant sense throughout lungfish evolution, and changes in the labyrinth may potentially reflect a change from nektonic to near-shore environmental niches. Phylogenetic implications show that endocranial form fails to support monophyly of the ‘chirodipterids’. Those with elongated crania similarly fail to form a distinct clade, suggesting these two paraphyletic groups have converged towards either head elongation or truncation driven by non-phylogenetic constraints.https://elifesciences.org/articles/73461dipnoiendocasttomographypalaeoneurologypalaeozoicPCA
spellingShingle Alice M Clement
Tom J Challands
Richard Cloutier
Laurent Houle
Per E Ahlberg
Shaun P Collin
John A Long
Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
eLife
dipnoi
endocast
tomography
palaeoneurology
palaeozoic
PCA
title Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
title_full Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
title_fullStr Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
title_full_unstemmed Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
title_short Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
title_sort morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution
topic dipnoi
endocast
tomography
palaeoneurology
palaeozoic
PCA
url https://elifesciences.org/articles/73461
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